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Fast and pervasive transcriptomic resilience and acclimation of extremely heat-tolerant coral holobionts from the northern Red Sea

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2021

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Savary, Romain
Barshis, Daniel J.
Evensen, Nicolas R.
Banc-Prandi, Guilhem
Fine, Maoz
Meibom, Anders

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Proceedings of the National Academy of Sciences of the United States of America. National Academy of Sciences. 2021, 118(19), e2023298118. ISSN 0027-8424. eISSN 1091-6490. Available under: doi: 10.1073/pnas.2023298118

Zusammenfassung

Corals from the northern Red Sea and Gulf of Aqaba exhibit extreme thermal tolerance. To examine the underlying gene expression dynamics, we exposed Stylophora pistillata from the Gulf of Aqaba to short-term (hours) and long-term (weeks) heat stress with peak seawater temperatures ranging from their maximum monthly mean of 27 °C (baseline) to 29.5 °C, 32 °C, and 34.5 °C. Corals were sampled at the end of the heat stress as well as after a recovery period at baseline temperature. Changes in coral host and symbiotic algal gene expression were determined via RNA-sequencing (RNA-Seq). Shifts in coral microbiome composition were detected by complementary DNA (cDNA)-based 16S ribosomal RNA (rRNA) gene sequencing. In all experiments up to 32 °C, RNA-Seq revealed fast and pervasive changes in gene expression, primarily in the coral host, followed by a return to baseline gene expression for the majority of coral (>94%) and algal (>71%) genes during recovery. At 34.5 °C, large differences in gene expression were observed with minimal recovery, high coral mortality, and a microbiome dominated by opportunistic bacteria (including Vibrio species), indicating that a lethal temperature threshold had been crossed. Our results show that the S. pistillata holobiont can mount a rapid and pervasive gene expression response contingent on the amplitude and duration of the thermal stress. We propose that the transcriptomic resilience and transcriptomic acclimation observed are key to the extraordinary thermal tolerance of this holobiont and, by inference, of other northern Red Sea coral holobionts, up to seawater temperatures of at least 32 °C, that is, 5 °C above their current maximum monthly mean.

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Fachgebiet (DDC)
570 Biowissenschaften, Biologie

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coral bleaching, microbiome, heat stress, gene expression profiling, metaorganism

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ISO 690SAVARY, Romain, Daniel J. BARSHIS, Christian R. VOOLSTRA, Anny CÁRDENAS, Nicolas R. EVENSEN, Guilhem BANC-PRANDI, Maoz FINE, Anders MEIBOM, 2021. Fast and pervasive transcriptomic resilience and acclimation of extremely heat-tolerant coral holobionts from the northern Red Sea. In: Proceedings of the National Academy of Sciences of the United States of America. National Academy of Sciences. 2021, 118(19), e2023298118. ISSN 0027-8424. eISSN 1091-6490. Available under: doi: 10.1073/pnas.2023298118
BibTex
@article{Savary2021-05-11perva-53963,
  year={2021},
  doi={10.1073/pnas.2023298118},
  title={Fast and pervasive transcriptomic resilience and acclimation of extremely heat-tolerant coral holobionts from the northern Red Sea},
  number={19},
  volume={118},
  issn={0027-8424},
  journal={Proceedings of the National Academy of Sciences of the United States of America},
  author={Savary, Romain and Barshis, Daniel J. and Voolstra, Christian R. and Cárdenas, Anny and Evensen, Nicolas R. and Banc-Prandi, Guilhem and Fine, Maoz and Meibom, Anders},
  note={Article Number: e2023298118}
}
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